The role of vital dietary biomolecules in eco-evo-devo dynamics
Authors: Libor Závorka, Andreu Blanco, Fernando Chaguaceda, Julien Cucherousset, Shaun S. Killen, Camilla Liénart, Margaux Mathieu-Resuge, Pavel Němec, Matthias Pilecky, Kristin Scharnweber, Cornelia W. Twining, Martin J. Kainz
Journal: Trends in Ecology & Evolution (2022)

Availability of vital dietary biomolecules, such as vitamins, amino acids, and fatty acids, is critical for the evolution and development of animals.Extensive evidence indicates that anthropogenic changes influence the distribution of vital dietary biomolecules in food webs.Shifts in the availability of these vital biomolecules can trigger far-reaching changes in phenotypes of consumers with potential cascading impacts on the functioning of the ecosystems.There is no unified integrative framework to study the role of vital dietary biomolecules in feedbacks between phenotypes of wild consumers and ecosystem functioning.We review evidence on omega-3 long-chain polyunsaturated fatty acids (n-3 LC-PUFA) in prey–predator interactions to illustrate how vital dietary biomolecules moderate the feedbacks between behavioral, physiological, and life-history traits of wild consumers and the higher levels of biological organization. The physiological dependence of animals on dietary intake of vitamins, amino acids, and fatty acids is ubiquitous. Sharp differences in the availability of these vital dietary biomolecules among different resources mean that consumers must adopt a range of strategies to meet their physiological needs. We review the emerging work on omega-3 long-chain polyunsaturated fatty acids, focusing predominantly on predator–prey interactions, to illustrate that trade-off between capacities to consume resources rich in vital biomolecules and internal synthesis capacity drives differences in phenotype and fitness of consumers. This can then feedback to impact ecosystem functioning. We outline how focus on vital dietary biomolecules in eco-eco-devo dynamics can improve our understanding of anthropogenic changes across multiple levels of biological organization. The physiological dependence of animals on dietary intake of vitamins, amino acids, and fatty acids is ubiquitous. Sharp differences in the availability of these vital dietary biomolecules among different resources mean that consumers must adopt a range of strategies to meet their physiological needs. We review the emerging work on omega-3 long-chain polyunsaturated fatty acids, focusing predominantly on predator–prey interactions, to illustrate that trade-off between capacities to consume resources rich in vital biomolecules and internal synthesis capacity drives differences in phenotype and fitness of consumers. This can then feedback to impact ecosystem functioning. We outline how focus on vital dietary biomolecules in eco-eco-devo dynamics can improve our understanding of anthropogenic changes across multiple levels of biological organization. Environmental changes induced by anthropogenic activities affect the flux and distribution of nutrients, including vital dietary biomolecules (see Glossary) such as thiamine [1.Ejsmond M.J. et al.Modeling vitamin B1 transfer to consumers in the aquatic food web.Sci. Rep. 2019; 9: 10045Crossref PubMed Scopus (12) Google Scholar] or omega-3 long-chain polyunsaturated fatty acid (n-3 LC-PUFA) [2.Hixson S.M. Arts M.T. Climate warming is predicted to reduce omega-3, long-chain, polyunsaturated fatty acid production in phytoplankton.Glob. Change Biol. 2016; 22: 2744-2755Crossref PubMed Scopus (127) Google Scholar], across ecosystems around the globe. The importance of these vital dietary biomolecules for consumer development has been thoroughly studied in veterinary and medical sciences, providing evidence of their role for animal health, reproduction, and neural tissue functioning (e.g., [3.Innis S.M. Dietary (n-3) fatty acids and brain development.J. Nutr. 2007; 137: 855-859Crossref PubMed Scopus (618) Google Scholar, 4.Kraft C.E. Angert E.R. Competition for vitamin B 1 (thiamin) structures numerous ecological interactions.Q. Rev. Biol. 2017; 92: 151-168Crossref PubMed Scopus (0) Google Scholar, 5.Stabler S.P. Vitamin B12 deficiency.N. Engl. J. Med. 2013; 368: 149-160Crossref PubMed Scopus (557) Google Scholar]). However, ecologists have rarely considered the substantial spatial [6.Guo F. et al.Longitudinal variation in the nutritional quality of basal food sources and its effect on invertebrates and fish in subalpine rivers.J. Anim. Ecol. 2021; 90: 2678-2691Crossref PubMed Scopus (5) Google Scholar,7.Colombo S.M. et al.A fundamental dichotomy in long-chain polyunsaturated fatty acid abundance between and within marine and terrestrial ecosystems.Environ. Rev. 2017; 25: 163-174Crossref Scopus (72) Google Scholar] and temporal [8.Fuiman L.A. Egg boon fatty acids reveal effects of a climatic event on a marine food web.Ecol. Monogr. 2018; 88: 585-599Crossref Scopus (11) Google Scholar,9.Shipley J.R. et al.Climate change shifts the timing of nutritional flux from aquatic insects.Curr. Biol. 2022; 32: 1342-1349Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar] variations in the availability of vital dietary biomolecules across the food webs. In addition, even closely related species and populations of consumers can differ in their physiological dependence on specific dietary biomolecules [10.Twining C.W. et al.Use of fatty acids from aquatic prey varies with foraging strategy.Front. Ecol. Evol. 2021; 9735350Crossref Scopus (5) Google Scholar] and their capacity to synthesize them internally when they are not available in the diet [11.Hudson C.M. et al.Fit and fatty freshwater fish: contrasting polyunsaturated fatty acid phenotypes between hybridizing stickleback lineages.Oikos. 2021; 2022: 1-14Google Scholar, 12.Ishikawa A. et al.Copy number variation of a fatty acid desaturase gene Fads2 associated with ecological divergence in freshwater stickleback populations.Biol. Lett. 2021; 17: 20210204Crossref PubMed Scopus (3) Google Scholar, 13.Ishikawa A. et al.(2019) A key metabolic gene for recurrent freshwater colonization and radiation in fishes.Science. 1979; 364: 886-889Crossref Scopus (68) Google Scholar]. Therefore, while energy is typically considered the common currency underlying numerous ecological and physiological phenomena, vital dietary biomolecules likely play the role of critically limiting commodities that are produced and transferred among consumers within and across food webs. Dietary biomolecules can be a key determinant of individual fitness and affect the functioning of ecosystems. Therefore, a greater focus on the role of vital dietary biomolecules in feedbacks between phenotypes of consumers and their environment, that is, eco-evo-devo dynamics, can improve our understanding of the effects of anthropogenic environmental changes across multiple levels of biological organization. There is, however, a notable lack of integrative work exploring the importance of vital dietary biomolecules in nature, causing researchers to overlook potentially critical links between the evolution and development of consumers and ecosystem functioning. The role of vital dietary biomolecules in the evolution and development of consumer phenotype is largely determined by the trade-off between the capacity of a consumer to acquire food sources rich in a given dietary biomolecule and its capacity to synthesize that same molecule internally or via endosymbiosis from more accessible dietary precursors [4.Kraft C.E. Angert E.R. Competition for vitamin B 1 (thiamin) structures numerous ecological interactions.Q. Rev. Biol. 2017; 92: 151-168Crossref PubMed Scopus (0) Google Scholar,14.Husnik F. Host–symbiont–pathogen interactions in blood-feeding parasites: nutrition, immune cross-talk and gene exchange.Parasitology. 2018; 145: 1294-1303Crossref PubMed Scopus (19) Google Scholar]. While many examples in this review concern predator–prey interactions, this trade-off is intrinsic to most consumers including parasites [14.Husnik F. Host–symbiont–pathogen interactions in blood-feeding parasites: nutrition, immune cross-talk and gene exchange.Parasitology. 2018; 145: 1294-1303Crossref PubMed Scopus (19) Google Scholar] and detritivores [15.Crenier C. et al.Minor food sources can play a major role in secondary production in detritus-based ecosystems.Freshw. Biol. 2017; 62: 1155-1167Crossref Scopus (40) Google Scholar]. The fact that many consumers do not simultaneously invest in both dietary acquisition and synthesis of vital biomolecules is likely driven by high energetic cost of synthesis [16.Cohen A.A. et al.Co-existence of multiple trade-off currencies shapes evolutionary outcomes.PLoS One. 2017; 12e0189124Crossref Scopus (17) Google Scholar,17.Maklakov A.A. Chapman T. Evolution of ageing as a tangle of trade-offs: energy versus function.Proc. R. Soc. B. 2019; 286: 20191604Crossref PubMed Scopus (0) Google Scholar]. Moreover, adaptation toward one end of this trade-off may relax selection pressure and lead to a loss of traits associated with the other [18.Lahti D.C. et al.Relaxed selection in the wild.Trends Ecol. Evol. 2009; 24: 487-496Abstract Full Text Full Text PDF PubMed Scopus (372) Google Scholar,19.Ellers J. et al.Ecological interactions drive evolutionary loss of traits.Ecol. Lett. 2012; 15: 1071-1082Crossref PubMed Scopus (78) Google Scholar]. Consumers can limit this trade-off by reducing their physiological dependence on a given dietary biomolecule. For example, by reducing growth of nutrient-demanding tissues, such as n-3 LC-PUFA-rich brain [3.Innis S.M. Dietary (n-3) fatty acids and brain development.J. Nutr. 2007; 137: 855-859Crossref PubMed Scopus (618) Google Scholar], or by adopting behavioral and physiological strategies that increase the retention of scarce dietary biomolecules [20.Olsen L. et al.Lipid metabolism in adaptation to extreme nutritional challenges.Dev. Cell. 2021; 56: 1417-1429Abstract Full Text Full Text PDF PubMed Scopus (0) Google Scholar]. However, reducing physiological dependence on vital dietary biomolecules in the short term can reduce the biological fitness of the consumer and limit its potential to adapt to environmental change [21.Raffard A. et al.The community and ecosystem consequences of intraspecific diversity: a meta-analysis.Biol. Rev. 2019; 94: 648-661Crossref PubMed Scopus (112) Google Scholar]. Importantly, these changes in consumer phenotype can then feedback to the functioning of ecosystems. Traits of consumers related to dietary acquisition and internal synthesis of the vital biomolecules (e.g., food source selectivity or organismal stoichiometry) likely have direct impacts on ecosystem functioning and thus can be considered functional effect traits, which determine the per-capita ecological impacts of consumers [21.Raffard A. et al.The community and ecosystem consequences of intraspecific diversity: a meta-analysis.Biol. Rev. 2019; 94: 648-661Crossref PubMed Scopus (112) Google Scholar,22.Dı́az S. Cabido M. Vive la différence: plant functional diversity matters to ecosystem processes.Trends Ecol. Evol. 2001; 16: 646-655Abstract Full Text Full Text PDF Scopus (0) Google Scholar] (Figure 1). Traits of consumers that drive the physiological need for specific dietary biomolecules (e.g., brain or gonad size) have direct impact on fitness of consumers and thus can be considered functional response traits that affect population growth and feedback to the community and ecosystem levels as density-dependent ecological effects [22.Dı́az S. Cabido M. Vive la différence: plant functional diversity matters to ecosystem processes.Trends Ecol. Evol. 2001; 16: 646-655Abstract Full Text Full Text PDF Scopus (0) Google Scholar,23.Hendry A.P. A critique for eco-evolutionary dynamics.Funct. Ecol. 2019; 33: 84-94Crossref Scopus (37) Google Scholar] (Figure 1). We summarize emerging evidence of the ecological, evolutionary, and developmental importance of vital dietary biomolecules using n-3 LC-PUFA as a specific example. While we focus on n-3 LC-PUFA, the general concepts that we cover can guide research of eco-evo-devo dynamics on numerous other vital biomolecules such as vitamins [24.Drouin G. et al.The genetics of vitamin C loss in vertebrates.Curr. Genom. 2011; 12: 371-378Crossref PubMed Google Scholar], sterols [25.Martin-Creuzburg D. et al.Colimitation of a freshwater herbivore by sterols and polyunsaturated fatty acids.Proc. R. Soc. B. 2009; 276: 1805-1814Crossref PubMed Scopus (100) Google Scholar], and amino acids [26.Nepi M. Beyond nectar sweetness: the hidden ecological role of non-protein amino acids in nectar.J. Ecol. 2014; 102: 108-115Crossref Scopus (66) Google Scholar], which are not as well studied from ecological and evolutionary perspectives as n-3 LC-PUFAs. At the biochemical level, n-3 LC-PUFAs are critical for functioning of cell membrane lipids which have direct impacts on the efficiency of signal transfer in tissues [27.Pilecky M. et al.Omega-3 PUFA profoundly affect neural, physiological, and behavioural competences – implications for systemic changes in trophic interactions.Biol. Rev. 2021; 96: 2127-2145Crossref PubMed Scopus (14) Google Scholar] (Box 1). This key biochemical function is why n-3 LC-PUFAs are important for a broad range of physiological [28.McKenzie D.J. Effects of dietary fatty acids on the respiratory and cardiovascular physiology of fish.Comp. Biochem. Physiol. A. 2001; 128: 605-619Crossref Google Scholar], cognitive [27.Pilecky M. et al.Omega-3 PUFA profoundly affect neural, physiological, and behavioural competences – implications for systemic changes in trophic interactions.Biol. Rev. 2021; 96: 2127-2145Crossref PubMed Scopus (14) Google Scholar], and life history [29.Hulbert A.J. Explaining longevity of different animals: is membrane fatty acid composition the missing link?.AGE. 2008; 30: 89-97Crossref PubMed Scopus (0) Google Scholar] traits. There are ecologically meaningful differences in the availability of n-3 LC-PUFA at the base of food webs at different spatial and temporal scales [7.Colombo S.M. et al.A fundamental dichotomy in long-chain polyunsaturated fatty acid abundance between and within marine and terrestrial ecosystems.Environ. Rev. 2017; 25: 163-174Crossref Scopus (72) Google Scholar,9.Shipley J.R. et al.Climate change shifts the timing of nutritional flux from aquatic insects.Curr. Biol. 2022; 32: 1342-1349Abstract Full Text Full Text PDF PubMed Scopus (11) Google Scholar]. Globally, the main source of dietary n-3 LC-PUFA is produced by aquatic primary producers [7.Colombo S.M. et al.A fundamental dichotomy in long-chain polyunsaturated fatty acid abundance between and within marine and terrestrial ecosystems.Environ. Rev. 2017; 25: 163-174Crossref Scopus (72) Google Scholar,30.Twining C.W. et al.Highly unsaturated fatty acids in nature: what we know and what we need to learn.Oikos. 2016; 125: 749-760Crossref Scopus (141) Google Scholar], and in some environments, also by bacteria [31.Nichols D.S. Prokaryotes and the input of polyunsaturated fatty acids to the marine food web.FEMS Microbiol. Lett. 2003; 219: 1-7Crossref PubMed Scopus (75) Google Scholar] and protists [32.Veloza A.J. et al.Trophic modification of essential fatty acids by heterotrophic protists and its effects on the fatty acid composition of the copepod Acartia tonsa.Mar. Biol. 2006; 148: 779-788Crossref Scopus (79) Google Scholar]. Omega-3 LC-PUFAs from aquatic primary producers are transferred to higher trophic levels [33.Kainz M. et al.Essential fatty acids in the planktonic food web and their ecological role for higher trophic levels.Limnol. Oceanogr. 2004; 49: 1784-1793Crossref Scopus (240) Google Scholar], and a large part of this aquatic production is transferred to terrestrial ecosystems [34.Fritz K.A. et al.Subsidies of long-chain polyunsaturated fatty acids from aquatic to terrestrial environments via amphibian emergence.Freshw. Biol. 2019; 64: 832-842Crossref Scopus (7) Google Scholar,35.Mathieu-Resuge M. et al.Taxonomic composition and lake bathymetry influence fatty acid export via emergent insects.Freshw. Biol. 2021; 66: 2199-2209Crossref Scopus (3) Google Scholar]. The availability of n-3 LC-PUFAs is generally higher in marine than in freshwater ecosystems [30.Twining C.W. et al.Highly unsaturated fatty acids in nature: what we know and what we need to learn.Oikos. 2016; 125: 749-760Crossref Scopus (141) Google Scholar,36.Twining C.W. et al.The evolutionary ecology of fatty-acid variation: implications for consumer adaptation and diversification.Ecol. Lett. 2021; 24: 1709-1731Crossref PubMed Scopus (24) Google Scholar]. It has been shown that the availability of n-3 LC-PUFAs within marine ecosystems is closely linked to the algal community assemblage [7.Colombo S.M. et al.A fundamental dichotomy in long-chain polyunsaturated fatty acid abundance between and within marine and terrestrial ecosystems.Environ. Rev. 2017; 25: 163-174Crossref Scopus (72) Google Scholar,37.Galloway A.W.E. Winder M. Partitioning the relative importance of phylogeny and environmental conditions on phytoplankton fatty acids.PLoS One. 2015; 10e0130053Crossref Scopus (162) Google Scholar]. There are numerous marine gradients in n-3 LC-PUFA availability with latitude, from poor oligotrophic open ocean to rich coastal upwelling systems, from rocky to sandy coasts, or from brackish estuary to salt marine waters [7.Colombo S.M. et al.A fundamental dichotomy in long-chain polyunsaturated fatty acid abundance between and within marine and terrestrial ecosystems.Environ. Rev. 2017; 25: 163-174Crossref Scopus (72) Google Scholar,37.Galloway A.W.E. Winder M. Partitioning the relative importance of phylogeny and environmental conditions on phytoplankton fatty acids.PLoS One. 2015; 10e0130053Crossref Scopus (162) Google Scholar,38.Winder M. et al.The land-sea interface: a source of high-quality phytoplankton to support secondary production.Limnol. Oceanogr. 2017; 62: S258-S271Crossref Scopus (29) Google Scholar]. In freshwater ecosystems, there is higher n-3 LC-PUFA availability in lentic than in lotic ecosystems [39.Heissenberger M. et al.Effect of nutrition on fatty acid profiles of riverine, lacustrine, and aquaculture-raised salmonids of pre-alpine habitats.Hydrobiologia. 2010; 650: 243-254Crossref Scopus (60) Google Scholar]. At finer spatial scales, n-3 LC-PUFA availability is greater in pelagic than in littoral areas of lentic ecosystems [40.Kainz M.J. et al.Polyunsaturated fatty acids in fishes increase with total lipids irrespective of feeding sources and trophic position.Ecosphere. 2017; 8: 13Crossref Scopus (31) Google Scholar,41.Scharnweber K. et al.Fatty acid accumulation in feeding types of a natural freshwater fish population.Oecologia. 2021; 196: 53-63Crossref PubMed Scopus (7) Google Scholar] and increases with stream order in lotic ecosystems as freshwater primary producers become the dominant source of energy [6.Guo F. et al.Longitudinal variation in the nutritional quality of basal food sources and its effect on invertebrates and fish in subalpine rivers.J. Anim. Ecol. 2021; 90: 2678-2691Crossref PubMed Scopus (5) Google Scholar]. In terrestrial ecosystems, the availability of dietary n-3 LC-PUFA for consumers generally decreases with the distance from aquatic ecosystems [10.Twining C.W. et al.Use of fatty acids from aquatic prey varies with foraging strategy.Front. Ecol. Evol. 2021; 9735350Crossref Scopus (5) Google Scholar]. Together, the heterogeneous spatiotemporal distribution of dietary n-3 LC-PUFA, a consumer's physiological dependence on n-3 LC-PUFA, and a consumer's position along the synthesis and acquisition trade-off create a strong selection gradient that can drive developmental and evolutionary changes in traits that have a direct impact on ecosystem functioning (Figure 1).Box 1Cellular function of n-3 LC-PUFAThe most physiologically important n-3 LC-PUFAs for many consumers are DHA (22:6n-3) and EPA (20:5n-3) and their short-chain precursor ALA (18:3n-3) [27.Pilecky M. et al.Omega-3 PUFA profoundly affect neural, physiological, and behavioural competences – implications for systemic changes in trophic interactions.Biol. Rev. 2021; 96: 2127-2145Crossref PubMed Scopus (14) Google Scholar,36.Twining C.W. et al.The evolutionary ecology of fatty-acid variation: implications for consumer adaptation and diversification.Ecol. Lett. 2021; 24: 1709-1731Crossref PubMed Scopus (24) Google Scholar]. LC-PUFAs increase the fluidity of cellular membranes due to their high rotation potential given by high number of unsaturated double bonds and chain length [113.Hazel J.R. Williams E.E. The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment.Prog. Lipid Res. 1990; 29: 167-227Crossref PubMed Scopus (765) Google Scholar]. The high rotation potential of DHA has a critical role in signal transfer efficiency in neural tissues of virtually all vertebrates, and a large number of aquatic invertebrates such as copepods, malacostraca, and cephalopods [27.Pilecky M. et al.Omega-3 PUFA profoundly affect neural, physiological, and behavioural competences – implications for systemic changes in trophic interactions.Biol. Rev. 2021; 96: 2127-2145Crossref PubMed Scopus (14) Google Scholar,36.Twining C.W. et al.The evolutionary ecology of fatty-acid variation: implications for consumer adaptation and diversification.Ecol. Lett. 2021; 24: 1709-1731Crossref PubMed Scopus (24) Google Scholar]. However, many freshwater invertebrates do not have DHA in their membrane lipids and its function is provided by EPA [6.Guo F. et al.Longitudinal variation in the nutritional quality of basal food sources and its effect on invertebrates and fish in subalpine rivers.J. Anim. Ecol. 2021; 90: 2678-2691Crossref PubMed Scopus (5) Google Scholar]. Furthermore, terrestrial invertebrates contain negligible amount of DHA and EPA and their neural tissue membrane lipid function is realized by ALA [114.Hixson S.M. et al.Long-chain omega-3 polyunsaturated fatty acids have developmental effects on the crop pest, the cabbage white butterfly Pieris rapae.PLoS One. 2016; 11e0152264Crossref PubMed Scopus (19) Google Scholar].The importance of these fatty acids in the cellular structure of consumers means that these lipids are not primarily oxidized for energy production, but are retained and incorporated into membranes or used for synthesis of n-3 LC-PUFA species required by the consumer (e.g., synthesis of DHA from ALA and EPA by vertebrates) [46.Castro L.F.C. et al.Long-chain polyunsaturated fatty acid biosynthesis in chordates: insights into the evolution of Fads and Elovl gene repertoire.Prog. Lipid Res. 2016; 62: 25-40Crossref PubMed Scopus (239) Google Scholar]. When consumers acquire more dietary n-3 LC-PUFA than needed to maintain optimal functioning of cellular membranes, they can store them for later use as triacylglycerols (TAGs) [115.Mathieu-Resuge M. et al.Specific regulations of gill membrane fatty acids in response to environmental variability reveal fitness differences between two suspension-feeding bivalves (Nodipecten subnodosus and Spondylus crassisquama).Conserv. Physiol. 2020; 8: coaa079Crossref PubMed Scopus (1) Google Scholar], retro-convert them to shorter chain (e.g., conversion of DHA and EPA to ALA by terrestrial insects [114.Hixson S.M. et al.Long-chain omega-3 polyunsaturated fatty acids have developmental effects on the crop pest, the cabbage white butterfly Pieris rapae.PLoS One. 2016; 11e0152264Crossref PubMed Scopus (19) Google Scholar] or DHA to EPA in Daphnia [116.Martin-Creuzburg D. et al.Interactions between limiting nutrients: consequences for somatic and population growth of Daphnia magna.Limnol. Oceanogr. 2010; 55: 2597-2607Crossref Scopus (68) Google Scholar]); or oxidize them to produce energy [117.Stanley-Samuelson W. et al.Fatty acids in insects: composition, metabolism, and biological significance.Arch. Insect Biochem. Physiol. 1988; 9: 1-33Crossref Scopus (374) Google Scholar]. Because excess dietary n-3 LC-PUFAs are stored or used as an energy source, an increase of n-3 LC-PUFA in diet above the physiological optimum is unlikely to improve functioning of consumer's cellular membranes and their fitness (Figure I) [38.Winder M. et al.The land-sea interface: a source of high-quality phytoplankton to support secondary production.Limnol. Oceanogr. 2017; 62: S258-S271Crossref Scopus (29) Google Scholar]. Excessive anthropogenic supply of n-3 LC-PUFAs (e.g., from genetically modified crops; see Figure 2 in main text) to consumers that utilize ALA as dominant membrane lipid (i.e., terrestrial insects) can cause developmental deformities [114.Hixson S.M. et al.Long-chain omega-3 polyunsaturated fatty acids have developmental effects on the crop pest, the cabbage white butterfly Pieris rapae.PLoS One. 2016; 11e0152264Crossref PubMed Scopus (19) Google Scholar], but the negative health effects of excessive n-3 LC-PUFA consumption (i.e., oversaturation) are not known in natural ecosystems. By contrast, dietary intake of n-3 LC-PUFA below the physiological optimum can have severe negative effects on the performance of consumers' tissues and ultimately their fitness (Figure I) [27.Pilecky M. et al.Omega-3 PUFA profoundly affect neural, physiological, and behavioural competences – implications for systemic changes in trophic interactions.Biol. Rev. 2021; 96: 2127-2145Crossref PubMed Scopus (14) Google Scholar,36.Twining C.W. et al.The evolutionary ecology of fatty-acid variation: implications for consumer adaptation and diversification.Ecol. Lett. 2021; 24: 1709-1731Crossref PubMed Scopus (24) Google Scholar]. The most physiologically important n-3 LC-PUFAs for many consumers are DHA (22:6n-3) and EPA (20:5n-3) and their short-chain precursor ALA (18:3n-3) [27.Pilecky M. et al.Omega-3 PUFA profoundly affect neural, physiological, and behavioural competences – implications for systemic changes in trophic interactions.Biol. Rev. 2021; 96: 2127-2145Crossref PubMed Scopus (14) Google Scholar,36.Twining C.W. et al.The evolutionary ecology of fatty-acid variation: implications for consumer adaptation and diversification.Ecol. Lett. 2021; 24: 1709-1731Crossref PubMed Scopus (24) Google Scholar]. LC-PUFAs increase the fluidity of cellular membranes due to their high rotation potential given by high number of unsaturated double bonds and chain length [113.Hazel J.R. Williams E.E. The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment.Prog. Lipid Res. 1990; 29: 167-227Crossref PubMed Scopus (765) Google Scholar]. The high rotation potential of DHA has a critical role in signal transfer efficiency in neural tissues of virtually all vertebrates, and a large number of aquatic invertebrates such as copepods, malacostraca, and cephalopods [27.Pilecky M. et al.Omega-3 PUFA profoundly affect neural, physiological, and behavioural competences – implications for systemic changes in trophic interactions.Biol. Rev. 2021; 96: 2127-2145Crossref PubMed Scopus (14) Google Scholar,36.Twining C.W. et al.The evolutionary ecology of fatty-acid variation: implications for consumer adaptation and diversification.Ecol. Lett. 2021; 24: 1709-1731Crossref PubMed Scopus (24) Google Scholar]. However, many freshwater invertebrates do not have DHA in their membrane lipids and its function is provided by EPA [6.Guo F. et al.Longitudinal variation in the nutritional quality of basal food sources and its effect on invertebrates and fish in subalpine rivers.J. Anim. Ecol. 2021; 90: 2678-2691Crossref PubMed Scopus (5) Google Scholar]. Furthermore, terrestrial invertebrates contain negligible amount of DHA and EPA and their neural tissue membrane lipid function is realized by ALA [114.Hixson S.M. et al.Long-chain omega-3 polyunsaturated fatty acids have developmental effects on the crop pest, the cabbage white butterfly Pieris rapae.PLoS One. 2016; 11e0152264Crossref PubMed Scopus (19) Google Scholar]. The importance of these fatty acids in the cellular structure of consumers means that these lipids are not primarily oxidized for energy production, but are retained and incorporated into membranes or used for synthesis of n-3 LC-PUFA species required by the consumer (e.g., synthesis of DHA from ALA and EPA by vertebrates) [46.Castro L.F.C. et al.Long-chain polyunsaturated fatty acid biosynthesis in chordates: insights into the evolution of Fads and Elovl gene repertoire.Prog. Lipid Res. 2016; 62: 25-40Crossref PubMed Scopus (239) Google Scholar]. When consumers acquire more dietary n-3 LC-PUFA than needed to maintain optimal functioning of cellular membranes, they can store them for later use as triacylglycerols (TAGs) [115.Mathieu-Resuge M. et al.Specific regulations of gill membrane fatty acids in response to environmental variability reveal fitness differences between two suspension-feeding bivalves (Nodipecten subnodosus and Spondylus crassisquama).Conserv. Physiol. 2020; 8: coaa079Crossref PubMed Scopus (1) Google Scholar], retro-convert them to shorter chain (e.g., conversion of DHA and EPA to ALA by terrestrial insects [114.Hixson S.M. et al.Long-chain omega-3 polyunsaturated fatty acids have developmental effects on the crop pest, the cabbage white butterfly Pieris rapae.PLoS One. 2016; 11e0152264Crossref PubMed Scopus (19) Google Scholar] or DHA to EPA in Daphnia [116.Martin-Creuzburg D. et al.Interactions between limiting nutrients: consequences for somatic and population growth of Daphnia magna.Limnol. Oceanogr. 2010; 55: 2597-2607Crossref Scopus (68) Google Scholar]); or oxidize them to produce energy [117.Stanley-Samuelson W. et al.Fatty acids in insects: composition, metabolism, and biological significance.Arch. Insect Biochem. Physiol. 1988; 9: 1-33Crossref Scopus (374) Google Scholar]. Because excess dietary n-3 LC-PUFAs are stored or used as an energy source, an increase of n-3 LC-PUFA in diet above the physiological optimum is unlikely to improve functioning of consumer's cellular membranes and their fitness (Figure I) [38.Winder M. et al.The land-sea i